Developmentally regulated alternative splicing of the α1(XI) collagen chain: Spatial and temporal segregation of isoforms in the cartilage of fetal rat long bones

Journal of Histochemistry and Cytochemistry

Volumn 48, Issue 6, 2000, Pages 725-741

  Morris, Nicholas P ^a,b,c   Oxford, Julia T ^a   Davies, Gillian B M ^a   Smoody, Barbara F ^a   Keene, Douglas R ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c SHRINERS HOSPITAL FOR CHILDREN   (United States)

Author keywords

Alternative splicing; Bone; Cartilage; Collagen; Isoforms; Localization; Skeletal development; Type XI

Indexed keywords

COLLAGEN;

ALTERNATIVE RNA SPLICING; AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CARTILAGE; EXON; GENE EXPRESSION; LONG BONE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; RAT;

ANIMALIA;

EID: 0034120662     PISSN: 00221554     EISSN: None     Source Type: Journal    
DOI: 10.1177/002215540004800601     Document Type: Article

References (55)

1. Archer CW, Morrison EH, Bayliss MT, Ferguson MW (1996) The development of articular cartilage: II. The spatial and temporal patterns of glycosaminoglycans and small leucine-rich proteoglycans.J Anat 189:23-35
2. Bianco P, Cancedda FD, Riminucci M, Cancedda R (1998) Bone formation via cartilage models: the "borderline" chondrocyte. Matrix Biol 17:185-192
3. Bianco P, Fisher LW, Young MF, Termine JD, Robey PG (1991) Expression of hone sialoprotein (BSP) in developing human tissues. Calcif Tissue Int 49:421-426
4. Bianco P, Riminucci M, Silvestrini G, Bonucci E, Termine JD, Fisher LW, Robey PG (1993) Localization of bone sialoprotein (BSP) to Golgi and post-Golgi secretory structures in osteoblasts and to discrete sites in early bone matrix. J Histochem Cytochem 41:193-203
5. Bland YS, Ashhurst DE (1996) Development and aging of the articular cartilage of the rabbit knee joint: distribution of the fibrillar collagens. Anat Embryol 194:607-619
6. Chazaud C, Bouillet P, Oulad-Abdelghani M, Dolle P (1996) Restricted expression of a novel retinoic acid responsive gene during limb bud dorsoventral patterning and endochondral ossification. Dev Genet 19:66-73
7. Clark G (1980) Miscellaneous methods. In Clark G, ed. Staining Procedures. 4th ed. Baltimore, Williams & Wilkins, 171-215
8. Coulter LR, Landree MA, Cooper TA (1997) Identification of a new class of exonic splicing enhancers by in vivo selection [published erratum appears in Mol Cell Biol 1997 Jun;17(6):3468]. Mol Cell Biol 17:2143-2150
9. Davies GBM, Oxford JT, Hausefus LW, Smoody BF, Morris NP (1998) Temporal and spatial expression of alternative splice-forms of the α1 (XI) collagen gene in fetal rat cartilage. Dev Dyn 213:12-26
10. Eikenherry BF, Mendler M, Burgin R, Winterhalter KH, Bruckner P (1992) Fibrillar organization in cartilage. In Kuettner K, ed. Articular Cartilage and Osteoarthritis. New York, Raven Press, 133-149
11. Eyre D, Wu J-J (1987) Type XI or 1α2α3α collagen. In Burgeson R, Mayne R, eds. Structure and Function of Collagen Types. Orlando, Academic Press, 261-281
12. Furuto DK, Miller EJ (1983) Different levels of glycosylation contribute to the heterogeneity of α1(II) collagen chains derived from a transplantable rat chondrosarcoma. Arch Biochem Biophys 226:604-611
13. Galotto M, Campanile G, Robino G, Cancedda FD, Bianco P, Cancedda R (1994) Hypertrophic chondrocytes undergo further differentiation to osteoblast-like cells and participate in the initial bone formation in developing chick embryo. J Bone Miner Res 9:1239-1249
14. Gerstenfeld LC, Shapiro FD (1996) Expression of bone-specific genes by hypertrophic chondrocytes: implications of the complex functions of the hypertrophic chondrocyte during endochondral bone development. J Cell Biochem 62:1-9
15. Keene DR, Lunstrum GP, Morris NP, Stoddard DW, Burgeson RE (1991) Two type XII-like collagens localize to the surface of banded collagen fibrils. J Cell Biol 113:971-978
16. Keene DR, Oxford JT, Morris NP (1995) Ultrastructural localization of collagen types II, IX, and XI in the growth plate of human rib and feral bovine epiphyseal cartilage: type XI collagen is restricted to thin fibrils. J Histochem Cytochem 43:967-979
17. Koyama E, Leatherman JL, Shimazu A, Nah H-D, Pacifici M (1995) Syndecan-3, tenascin-C, and the development of cartilaginous skeletal elements and joints in chick limbs. Dev Dyn 203:152-162
18. Lanske B, Karaplis AC, Lee K, Luz A, Vortkamp A, Pirro A, Karperien M, Defize LHK, Ho C, Mulligan RC, Abdul-Samra A-B, Juppner H, Segre GV, Kronenberg HM (1996) PTH/PTHrP receptor in early development and indian hedgehog-regulated bone growth. Science 273:663-666
19. Li Y, Lacerda DA, Warman ML, Beier DR, Yoshioka H, Ninomiya Y, Oxford JT, Morris NP, Andrikopoulos K, Ramirez F, Wardell BB, Lifferth GD, Teuscher C, Woodward SR, Taylor BA, Seegmiller RE, Olsen BR (1995) A fibrillar collagen gene, Coll 1a1, is essential for skeletal morphogenesis. Cell 80:423-430
20. Long F, Linsenmayer TF (1998) Regulation of growth region cartilage proliferation and differentiation by perichondrium. Development 125:1067-1073
21. Lui VCH, Kong RYC, Nicholls J, Cheung ANY, Cheah KSE (1995a) The mRNAs for the three chains of human collagen type XI are widely distributed but not necessarily co-expressed: implications for homotrimeric, heterotrimeric and heterotypic collagen molecules. Biochem J 311:511-516
22. Lui VCH, Ng LJ, Nicholls J, Tarn PPL, Cheah KSE (1995b) Tissue-specific and differential expression of alternatively spliced alpha I (II) collagen mRNAs in early human embryos. Dev Dyn 203:198-211
23. Macias D, Ganan Y, Sampath TK, Piedra ME, Ros MA, Hurle JM (1997) Role of BMP-2 and OP-1 (BMP-7) in programmed cell death and skeletogenesis during chick limb development. Development 124:1109-1117
24. Mendler M, Eich-Bender SG, Vaughan L, Winterhalter KH, Bruckner P (1989) Cartilage contains mixed fibrils of collagen types II, IX, and XI. J Cell Biol 108:191-197
25. Muro AF, Iaconcig A, Baralle FE (1998) Regulation of the fibronecrin EDA exon alternative splicing. Cooperative role of the exonic enhancer element and the 5′ splicing site. FEBS Lett 437:137-141
26. Neame PJ, Young CN, Treep JT (1990) Isolation and primary structure of PARP, a 24-kDa proline- and arginine-rich protein from bovine cartilage closely related to the NH2-terminal domain in collagen α1 (XI). J Biol Chem 265:20401-20408
27. Ng L, Tarn P, Cheah K (1993) Preferential expression of alternatively spliced mRNAs encoding type II procollagen with a cysteine-rich amino-propeptide in differentiating cartilage and non-chondrogenic tissues during early mouse development. Dev Biol 139:403-417
28. Oganesian A, Zhu Y, Sandell LJ (1997) Type IIA procollagen amino propeptide is localized in human embryonic tissues. J Histochem Cytochem 45:1469-1480
29. Oxford JT, Doege KJ, Norton WE, Morris NP (1994) Characterization of type II and type XI collagen synthesis by an immortalized rat chondrocyie cell line (IRC) having a low level of type II collagen mRNA expression. Exp Cell Res 213:28-36
30. Oxford JT, Doege KJ, Morris NP (1993) Alternative exon splicing within the ammo-terminal nontriple-helical domain of the rat pro-α1(XI) collagen chain generates multiple forms of the mRNA transcript which exhibit tissue-dependent variation. J Biol Chem 270:9478-9485
31. Pacifici M (1993) Tenascin-C and the development or articular cartilage. Matrix Biol 14:689-698
32. Ramirez F, Boast S, D'Alessio M, Lee B, Prince J, Su M, Vissing H, Yoshioka H (1990) Fibrillar collagen genes. Structure and expression in normal and diseased states. Ann NY Acad Sci 580:74-80
33. Rooney P, Archer CW (1992) The development of the perichondrium in the avian ulna. J Anat 181:393-401
34. Rousseau JC, Farjanel J, Boutillon MM, Hartmann DJ, Vanderrest M, Moradiameli M (1996) Processing of type XI collagen - processing of the matrix forms of the alpha 1(XI) chain. J Biol Chem 271:23743-23748
35. Sakai LY, Keene DR, Engvall E (1986) Fibrillin, a new 350-kD glycoprotein, is a component of extracellular microfibrils. J Cell Biol 103:2499-2309
36. Sandell LJ, Morris NP, Robbins JR, Goldring MB (1991) Alternatively spliced type II procollagen mRNAs define distinct populations of cells during vertebral development: differential expression of the amino-propeptide. J Cell Biol 114:1307-1319
37. Sandell LJ, Nalin AM, Reife RA (1994) Alternative splice form of type II procollagen mRNA (IIA) is predominant in skeletal precursors and non-cartilaginous tissues during early mouse development. Dev Dyn 199:129-140
38. Sato Y, Mukai K, Watanabe S, Goto M, Shimosato Y (1986) The AMeX method. A simplified technique of tissue processing and paraffin embedding with improved preservation of antigens for immunostaining. Am J Pathol 125:431-433
39. Schmid TM, Linsenmayer TF (1983) Immunohistochemical localization of short chain cartilage collagen (type X) in avian tissues. J Cell Biol 100:598-605
40. Serra R, Johnson M, Filvaroff EH, LaBorde J, Sheehan DM, Derynck R, Moses HL (1997) Expression of a truncated, kinase-defective TGF-beta type II receptor in mouse skeletal tissue promotes terminal chondrocyte differentiation and osteoarthritis. J Cell Biol 139:541-552
41. St-Jacques B, Hammerschmidt M, McMahon AP (1999) Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for hone formation. Genes Dev 13:2072-2086
42. Storm EE, Kingsley DM (1999) GDF5 coordinates bone and joint formation during digit development. Dev Biol 209:11-27
43. Sugimoto M, Kimura T, Tsumaki N, Matsui Y, Nakata K, Kawahata H, Yasui N, Kitamura Y, Nomura S, Ochi T (1998) Differential in situ expression of a2(XI) collagen mRNA isoforms in the developing mouse. Cell Tissue Res 292:325-332
44. Tacke R, Tohyama M, Ogawa S, Manley JL (1998) Human Tra2 proteins are sequence-specific activators of pre-mRNA splicing. Cell 93:139-148
45. Thom J, Morris N (1991) Biosynthesis and proteolytic processing of type XI collagen in embryonic chick sterna. J Biol Chem 266:7262-7269
46. Tian H, Kole R (1995) Selection of novel exon recognition elements from a pool of random sequences. Mol Cell Biol 15:6291-6298
47. Tsumaki N, Kimura T (1995) Differential expression of an acidic-domain in the amino-terminal propeptide of mouse pro-alpha 2(XI) collagen by complex alternative splicing. J Biol Chem 270:2372-2378
48. von Schroeder HP, Heersche JN (1998) Retinoic acid responsiveness of cells and tissues in developing fetal limbs evaluated in a RAREhsplacZ transgenic mouse model. J Orthop Res 16:355-364
49. Vortkamp A, Lee K, Lanske B, Segre GV, Kronenberg HM, Tabin CJ (1996) Regulation of rate of cartilage differentiation by indian hedgehog and PTH-related protein. Science 273:613-622
50. Watt SL, Lunstrum GP, McDonough AM, Keene DR, Burgeson RE, Morris NP (1992) Characterization of collagen types XII and XIV from fetal bovine cartilage. J Biol Chem 267:20093-20099
51. Yoshioka H, lyama K, Inoguchi K, Khaleduzzaman M, Ninomiya Y, Ramirez F (1995) Developmental pattern of expression of the mouse alpha-1(XI) collagen gene (Col 1 1a1). Dev Dyn 204:41-47
52. Yoshioka H, Ramirez F (1990) Pro-α1(XI) collagen. J Biol Chem 265:6423-6426
53. Zhidkova NI, Brewton RG, Mayne R (1993) Molecular cloning of PARP (proline/arginine-rich protein) from human cartilge and subsequent demonstration that PARP is a fragment of the NH2-terminal domain of collagen α2(XI) chain. FEBS Lett 326:25-28
54. Zhidkova NI, Justice SK, Mayne R (1995) Alternative mRNA processing occurs in the variable region of the pro-alpha 1(XI) and pro-alpha 2(XI) collagen chains. J Biol Chem 270:9486-9493
55. Zhu Y, Oganesian A, Keene DR, Sandell LJ (1999) Type IIA procollagen containing the cysteine-rich amino propeptide is deposited in the extracellular matrix of prechondrogenic tissue and binds to TGF-beta1 and BMP-2. J Cell Biol 144:1069-1080